Original
Abstract: The aim of this study was to evaluate the compared with the control group.
effects of the remnants of two suture materials on (J Oral Sci 57, 219-227, 2015)
osseointegration of titanium implants in a rabbit tibial
model. Calibrated defects were prepared in the tibia Keywords: suture materials; chitosan; nylon;
of five Chinchilla rabbits. Filaments of nonresorbable dental implants; bone; wound healing;
(NR) nylon or resorbable (R) chitosan were placed at osseointegration; biological complications.
the bone to implant interface, whereas control sites had
no suture material. After a healing period of 4 weeks,
a pull-out test procedure was performed followed by Introduction
enzymatic analyses of the wound fluid and relative Foreign materials, such as cement remnants from the
quantification of mRNA levels for bone-related and supraconstruction, can sometimes lead to peri-implant
cytokine markers from the peri-implant bone. A trend tissue complications (1). Theoretically, suture remnants
toward a reduced pull-out force was observed in the displaced toward the peri-implant bone may have a similar
NR group (NR: 23.0 ± 12.8 N; R: 33.9 ± 11.3 N; control: negative effect on the peri-implant tissues. The choice of
33.6 ± 24.0 N). Similarly, the bone resorption marker suture material may potentially influence the outcome
vacuolar type H+-ATPase was increased in the NR of periodontal and implant procedures (2,3). The ideal
group compared with that in the control group (P = suture material should provide uncomplicated stable
0.041). The R group showed trends for lower alkaline primary wound closure without affecting the treatment
phosphatase activity and osteocalcin expression and outcome negatively. However, suture materials often
higher total protein content and RNA compared with seem to worsen the inflammatory response for a variety
the control group. In this submerged healing model, of reasons (4); therefore, the selection of an appropriate
peri-implant bone healing was marginally affected by material is important (5,6). Materials that minimize
the two suture materials tested. However, there was inflammatory reactions are preferred, particularly in an
a tendency toward better osseointegration and lower environment, such as the oral cavity, where microbial
expression of bone resorption markers in the R group levels are high. Moreover, suture materials and their
metabolites might affect the healing process, particularly
after implant placement, and can also provide a route for
Correspondence to Dr. Johan Caspar Wohlfahrt, Department of communication between the fixture and the oral cavity
Biomaterials, Institute of Clinical Dentistry, University of Oslo,
P.O. Box 1109, Blindern, NO-0317 Oslo, Norway (2). Moreover, the wicking effect of some suture types
E-mail: j.c.wohlfahrt@odont.uio.no can result in harbouring and transporting bacteria to
doi.org/10.2334/josnusd.57.219 the depth of the wound; thus, evading the host defense
DN/JST.JSTAGE/josnusd/57.219 mechanism, resulting in local infection and subsequent
220
whether shear forces skewed the test from the load versus
displacement plot recorded. An immediate drop in the
curve indicated little influence of shear forces, whereas a
tapering curve indicated a greater influence.
Fig. 5 ALP activity, total protein, and specific ALP activity (corrected by total protein) measured in the wound
fluid collected from the implant site. Total protein content (expressed in microgram) extracted from each defect.
Values represent mean ± SEM (n = 5). ALP, alkaline phosphatase; CTRL, control; NR, nonresorbable monofila-
ments; R, resorbable monofilaments.
Fig. 7 In vivo expression of bone formation related markers (BMP-2, Coll-1, and OC), and a bone repair marker
(IGF-1). Data represent fold changes of target genes normalized with reference genes (18S, GAPDH, β-actin),
expressed as a percentage of the control group set at 100%. Values represent the mean ± SEM (n = 5). BMP-2,
bone morphogenetic protein-2; Coll-1, collagen-type 1; CTRL, control; GAPDH, glyceraldehyde-3-phosphate
dehydrogenase; IGF, insulin-like growth factor-1; NR, nonresorbable monofilaments; OC, osteocalcin; R, resorb-
able monofilaments.
Fig. 8 In vivo expression of bone resorption related markers (H+-ATPase, TRAP, and CalcR). Data represent
fold changes of target genes normalized with reference genes (18S, GAPDH, β-actin), expressed as a percentage
of the control group set at 100%. Values represent the mean ± SEM (n = 5). CTRL, control; GAPDH, glyceral-
dehyde-3-phosphate dehydrogenase; NR, nonresorbable monofilaments; R, resorbable monofilaments; TRAP,
tartrate-resistant acid phosphatase.
Fig. 9 In vivo expression of inflammatory markers (TNF-α, IL-6, and IL-10). Data represent fold changes of
target genes normalized with reference genes (18S, GAPDH, β-actin), expressed as a percentage of the control
group set to 100%. Values represent mean ± SEM (n = 5). CTRL, control; GAPDH, glyceraldehyde-3-phosphate
dehydrogenase; IL, interleukin; NR, nonresorbable monofilaments; R, resorbable monofilaments; TNF-α, tumor
necrosis factor-α.
at the bone-implant interface decreased implant retention OC expression, but this did not influence the outcome
to a greater extent than other groups and also resulted of the biomechanical test used to assess bone-implant
in statistically significant higher gene expression of attachment.
the bone resorption marker H+-ATPase. The R group Although tissue reactions around nylon monofilament
showed a trend toward lower specific ALP activity and sutures have been reported to be minimal (30), they can
225
elicit a foreign body tissue reaction in certain clinical the higher tissue reactivity and proteolytic enzymatic
situations (31,32). In our study, visual inspection of the degradation shown by the R material used in the present
bone defects after implant removal and measurement of experiment. Thus, biodegradation of chitosan fibers may
LDH activity indicated that nylon sutures did not induce lead to a specific cell response that can influence healing
any adverse reactions at the bone-implant interface. in the peri-implant tissues. Chou et al. (16) found that
However, nylon suture remnants showed a trend toward chitosan-treated macrophages decreased expression of
decreased implant attachment compared with chitosan pro-inflammatory cytokines (TNF-α and IL-6). In the
monofilaments. Moreover, increased gene expression of present study, a trend toward reduction of TNF-α and
H+-ATPase was observed in the nylon group. The vacuolar- IL-6 was also found in the chitosan group. Moreover,
type proton pump (H+-ATPase) is present in the ruffled a trend toward reduced expression of IL-10 was found
membrane of osteoclasts and is involved in osteoclastic in our study, while increased production of IL-10 by
bone resorption (33). Thus, the lower implant retention macrophages was reported by Chou et al. (16). Chitosan-
observed in the NR group may be related to higher bone coated culture plates have been reported to upregulate
resorption at the bone-implant interface. This might be genes associated with Coll-1, osteopontin, osteonectin,
explained by the nature of the nylon sutures used in the and OC in osteoblasts (38). Similarly, it has been shown
present experiment. The presence of NR filaments at that chitosan-coated fibers increased cell attachment,
the bone-implant interface may interfere with the initial ALP activity, and the expression of osteopontin on pre-
phase of bone healing, and histological evaluation could osteoblasts, resulting in significant mineralization in a
provide further insight into the osseointegration process 3D construct (39) and new bone formation in a rabbit
taking place at the interface. In the present study, the calvarial model (40). Our in vivo experiment differs from
bone-implant interface was disrupted on extraction of the the in vitro results from Matthews et al. (38) and Yang et
implants, and the samples were processed for enzymatic al. (39) as the expression of Coll-1 was not modified, the
and molecular analyses. Therefore, histological analysis specific ALP activity was reduced, and a trend toward
of the intact interface could not be carried out. reduction in the expression of OC was found. OC is a
The chitosan-based R suture material used in this marker for mineralization (41) and has been associated
study was still present in all defects, except for one site, with osseointegration (37). Thus, this observed trend
after a healing period of 4 weeks. The degradation time might be related to an ongoing remodeling in the peri-
of the chitosan material in this closed environment may implant bone tissue that takes place during the resorption
be longer than in an inflamed highly vascularized soft process of the suture material.
tissue. Some R suture materials require longer periods to This study examined the effects of suture materials
degrade, even in infected or acidic environments (6,34). on early wound healing and showed that sutures may
As reviewed by Pillai et al. (35), several modifications influence early peri-implant healing if filaments are left
can be made to the polymerization degree and polymer in close proximity to the bone-implant interface. Further
structure of chitosan such as etherification, esterifica- investigations are required to determine the influence of
tion, cross-linking, and grafting copolymerization to a broader number of sutures materials on peri-implant
enhance solubility. Moreover, the biodegradability of bone healing.
chitosan fibers increases with degree of acetylation (36).
All these parameters should be taken into consideration Acknowledgments
when selecting a suture for implant surgical procedures. This work was supported by the University of Oslo, the Norwe-
Although a suture with faster biodegradation rate might gian Research Council and the Ministerio de Ciencia e Innovación
be preferable when suturing peri-implant tissues, it may del Gobierno de España (Ramón y Cajal contract to MM) and
result in rapid resorption at the wound causing loss of NILS Science and Sustainability Programme (ES07 EEA Grants;
wound stability that can potentially affect the osseointe- 013-Abel-CM-2013). The authors have no conflicts of interest to
gration process. Moreover, the degradation process leads declare.
to different degrees of inflammatory response depending
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